Departamento de Biología, Facultad de Ciencias, Universidad Autónoma de Madrid, Madrid, Spain.
Vavilov Institute of General Genetics, Russian Academy of Sciences, Moscow, Russia.
Chromosoma. 2021 Sep;130(2-3):113-131. doi: 10.1007/s00412-021-00755-y. Epub 2021 Apr 6.
Sex determination in mammals is usually provided by a pair of chromosomes, XX in females and XY in males. Mole voles of the genus Ellobius are exceptions to this rule. In Ellobius tancrei, both males and females have a pair of XX chromosomes that are indistinguishable from each other in somatic cells. Nevertheless, several studies on Ellobius have reported that the two X chromosomes may have a differential organization and behavior during male meiosis. It has not yet been demonstrated if these differences also appear in female meiosis. To test this hypothesis, we have performed a comparative study of chromosome synapsis, recombination, and histone modifications during male and female meiosis in E. tancrei. We observed that synapsis between the two X chromosomes is limited to the short distal (telomeric) regions of the chromosomes in males, leaving the central region completely unsynapsed. This uneven behavior of sex chromosomes during male meiosis is accompanied by structural modifications of one of the X chromosomes, whose axial element tends to appear fragmented, accumulates the heterochromatin mark H3K9me3, and is associated with a specific nuclear body that accumulates epigenetic marks and proteins such as SUMO-1 and centromeric proteins but excludes others such as H3K4me, ubiH2A, and γH2AX. Unexpectedly, sex chromosome synapsis is delayed in female meiosis, leaving the central region unsynapsed during early pachytene. This region accumulates γH2AX up to the stage in which synapsis is completed. However, there are no structural or epigenetic differences similar to those found in males in either of the two X chromosomes. Finally, we observed that recombination in the sex chromosomes is restricted in both sexes. In males, crossover-associated MLH1 foci are located exclusively in the distal regions, indicating incipient differentiation of one of the sex chromosomes into a neo-Y. Notably, in female meiosis, the central region of the X chromosome is also devoid of MLH1 foci, revealing a lack of recombination, possibly due to insufficient homology. Overall, these results reveal new clues about the origin and evolution of sex chromosomes.
哺乳动物的性别决定通常由一对染色体决定，XX 染色体为雌性，XY 染色体为雄性。然而，白足鼠属的鼹形田鼠却是个例外。在白足田鼠中，雄性和雌性都有一对 XX 染色体，在体细胞中彼此无法区分。然而，几项针对白足田鼠的研究报告称，在雄性减数分裂过程中，这两条 X 染色体可能具有不同的组织和行为。目前尚不清楚这些差异是否也会出现在雌性减数分裂中。为了验证这一假设，我们对 E. tancrei 的雄性和雌性减数分裂过程中的染色体联会、重组和组蛋白修饰进行了比较研究。我们观察到，两条 X 染色体之间的联会仅限于染色体的短的远端（端粒）区域，而中央区域完全未联会。这种性染色体在雄性减数分裂过程中的不均匀行为伴随着一条 X 染色体的结构修饰，其轴丝倾向于出现碎片化，积累异染色质标记 H3K9me3，并与一个特定的核体结合，该核体积累组蛋白修饰和蛋白质，如 SUMO-1 和着丝粒蛋白，但排除其他如 H3K4me、ubih2A 和 γH2AX。出乎意料的是，性染色体联会在雌性减数分裂中延迟，使得早期粗线期中央区域未联会。该区域积累 γH2AX，直到联会完成。然而，在两条 X 染色体中，都没有类似于在雄性中发现的结构或表观遗传差异。最后，我们观察到，性染色体上的重组在两性中都受到限制。在雄性中，交叉相关的 MLH1 焦点仅位于远端区域，表明其中一条性染色体开始分化为一个新的 Y 染色体。值得注意的是，在雌性减数分裂中，X 染色体的中央区域也没有 MLH1 焦点，表明缺乏重组，可能是由于同源性不足。总的来说，这些结果揭示了关于性染色体起源和进化的新线索。
